Convergence of CpG DNA- and BCR- mediated signals at the c-Jun N-terminal kinase and NF-κB activation pathways: Regulation by mitogen-activated protein kinases

International Immunology

Volumn 15, Issue 5, 2003, Pages 577-591

  Yi, Ae Kyung ^a   Yoon, Jae Geun ^a   Krieg, Arthur M ^b,c  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c PFIZER INC   (United States)

Author keywords

Apoptosis; B Lymphocyte; BCR; CpG DNA; Cytokine; Protein kinase

Indexed keywords

B LYMPHOCYTE RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN M ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL MATURATION; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME INDUCTION; GROWTH DISORDER; LYMPHOCYTE PROLIFERATION; LYMPHOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPLEEN;

ANIMALS; CPG ISLANDS; DNA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LYMPHOMA, B-CELL; MAP KINASE KINASE KINASES; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION;

EID: 0037408105     PISSN: 09538178     EISSN: None     Source Type: Journal    
DOI: 10.1093/intimm/dxg058     Document Type: Article

References (59)

1. Janeway, C. A., Travers, P., Walport, M. and Capra, J. D. 1999. Signaling through lymphocyte receptors. In Immunobiology: The Immune System in Health and Disease, 4th edn, p. 163. Current Biology Publications, San Francisco, CA.
2. Cooke, M. P., Heath, A. W., Shokat, K. M., Zeng, Y., Finkelman, F. D., Linsley, P. S., Howard, M. and Goodnow, C. C. 1994. Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J. Exp. Med. 179:425.
3. Sproul, T. W., Malapati, S., Kim, J. and Pierce, S. K. 2000. B cell antigen receptor signaling occurs outside lipid rafts in immature B cells. J. Immunol. 165:6020.
4. Lee, H., Ausura, M., Wu, M., Duyao, M., Buckler, A. J. and Sonenshein, G. E. 1995. Role of Rel-related factors in control of c-myc gene transcription in receptor-mediated apoptosis of the murine B cell WEHI-231 line. J. Exp. Med. 181:1169.
5. Sutherland, C. L., Heath, A. W., Pelech, S. L., Young, P. R. and Gold, M. R. 1996. Differential activation of the ERK, JNK, and p38 mitogen-activated protein kinases by CD40 and the B cell antigen receptor. J. Immunol. 157:3381.
6. Healy, J. I., Dolmetsch, R. E., Timmerman, L. A., Cyster, J. G., Thomas, M. L., Crabtree, G. R., Lewis, R. S. and Goodnow, C. C. 1997. Different nuclear signals are activated by the B cell receptor during positive versus negative signaling. Immunity 6:419.
7. Goodnow, C. C. 1996. Balancing immunity and tolerance: deleting and tuning lymphocyte repertoires. Proc. Natl Acad. Sci. USA 93:2264.
8. Razin, A. and Friedman, J. 1981. DNA methylation and its possible biological roles. Prog. Nucleic Acid Res. Mol. Biol. 25:33.
9. Krieg, A. M., Yi, A.-K., Matson, S., Waldscmidt, T., Bishop, G., Teasdale, R., Koretzky, G. A. and Klinman, D. 1995. CpG motifs in bacterial DNA trigger direct B cell activation. Nature 374:546.
10. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K. and Akira, S. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740.
11. Stacey, K. J., Sweet, M. J. and Hume, D. A. 1996. Macrophages ingest and are activated by bacterial DNA. J. Immunol. 157:2116.
12. h1 response. J. Immunol. 168:4711.
13. Cowdery, J. S., Chace, J. H., Yi, A.-K. and Krieg, A. M. 1996. Bacterial DNA induces NK cells to produce interferon-gamma in vivo and increases the toxicity of lipopolysaccharides. J. Immunol. 156:4570.
14. Yi, A.-K., Tuetken, R., Redford, T., Waldschmidt, M., Kirsch, J. and Krieg, A. M. 1998. CpG motifs in bacterial DNA activate leukocytes through the pH-dependent generation of reactive oxygen species. J. Immunol. 160:4755.
15. Sparwasser, T., Koch, E. S., Vabulas, R. M., Heeg, K., Lipford, G. B., Ellwart, J. W. and Wagner, H. 1998. Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur. J. Immunol. 28:2045.
16. h1 responses by immunostimulatory DNA. J. Immunol. 161:3042.
17. Hartmann, G., Weiner, G. J. and Krieg, A. M. 1999. CpG DNA: a potent signal for growth, activation, and maturation of human dendritic cells. Proc. Natl Acad. Sci. USA 96:9305.
18. Yi, A.-K., Yoon, J.-G., Hong, S.-C., Redford, T. W. and Krieg, A. M. 2001. Lipopolysaccharide and CpG DNA synergize for tumor necrosis factor-α production through activation of NF-κB. Int. Immunol. 13:1391.
19. Krug, A., Rothenfusser, S., Hornung, V., Jahrsdorfer, B., Blackwell, S., Ballas, Z. K., Endres, S., Krieg, A. M. and Hartmann, G. 2001. Identification of CpG oligonucleotide sequences with high induction of IFN-alpha/beta in plasmacytoid dendritic cells. Eur. J. Immunol. 31:2154.
20. Yamamoto, S., Yamamoto, T., Kataoka, T., Kuramoto, E., Yano, O. and Tokunaga, T. 1992. Unique palindromic sequences in synthetic oligonucleotides are required to induce IFN and augment IFN-mediated natural killer activity. J. Immunol. 148:4072.
21. Yamamoto, T., Yamamoto, S., Kataoka, T. and Tokunaga, T. 1994. Lipofection of synthetic oligodeoxyribonucleotide having a palindromic sequence of AACGTT to murine splenocytes enhances interferon production and natural killer activity. Microbial Immunol. 38:831.
22. Ballas, Z. K., Rasmussen, W. L. and Krieg, A. M. 1996. Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleotides and bacterial DNA. J. Immunol. 157:1840.
23. Iho, S., Yamamoto, T., Takahashi, T. and Yamamoto, S. 1999. Oligodeoxynucleotides containing palindrome sequences with internal 5′-CpG-3′ act directly on human NK and activated T cells to induce IFN-γ production in vitro. J. Immunol. 163:3642.
24. Yi, A.-K., Klinman, D. M., Martin, T. L., Matson, S. and Krieg, A. M. 1996. Rapid immune activation by CpG motifs in bacterial DNA: systemic induction of IL-6 transcription through an antioxidant-sensitive pathway. J. Immunol. 157:5394.
25. Klinman, D. M., Yi, A.-K., Beaucage, S. L., Conover, J. and Krieg, A. M. 1996. CpG motifs present in bacterial DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon γ. Proc. Natl Acad. Sci. USA 93:2879.
26. Yi, A.-K., Chace, J. H., Cowdery, J. S. and Krieg, A. M. 1996. IFN-γ promotes IL-6 and IgM secretion in response to CpG motifs in bacterial DNA and oligodeoxynucleotides. J. Immunol. 156:558.
27. L. J. Immunol. 157:4918.
28. Yi, A.-K. and Krieg, A. M. 1998. CpG DNA rescue from anti-IgM induced WEHI-231 B lymphoma apoptosis via modulation of IκBα and IκBβ and sustained activation of nuclear factor-κB/c-Rel. J. Immunol. 160:1240.
29. Yi, A.-K., Chang, M., Peckham, D. W., Krieg, A. M. and Ashman, R. F. 1998. CpG oligodeoxyribonucleotides rescue mature murine spleen B cells from spontaneous apoptosis and promote cell cycle entry. J. Immunol. 160:5898.
30. Yi, A.-K., Peckham, D. W., Ashman, R. F. and Krieg, A. M. 1999. CpG DNA rescues B cells from apoptosis by activating NFκB and preventing mitochondrial membrane potential disruption via a chloroquine sensitive pathway. Int. Immunol. 11:2015.
31. Leadbetter, E. A., Rifkin, I. R., Hohlbaum, A. M., Beaudette, B. C., Shlomchik, M. J. and Marshak-Rothstein, A. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416:603.
32. Sandel, P. C. and Monroe, J. G. 1999. Negative selection of immature B cells by receptor editing or deletion is determined by site of antigen encounter. Immunity 10:289.
33. Yi, A.-K. and Krieg, A. M. 1998. Rapid induction of mitogen activated protein kinases by immune stimulatory CpG DNA. J. Immunol. 161:4493.
34. Derijard, B., Raingeaud, J., Barrett, T., Wu, I.-H., Han, J., Ulevitch, R. J. and Davis, R. J. 1995. Independent human MAP kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267:682.
35. Raingeaud, J., Whitmarsh, A. J., Barrett, T., Derijard, B. and Davis, R. J. 1996. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell. Biol. 16:1247.
36. Tibbles, L. A., Ing, Y. L., Kiefer, F., Chan, J., Iscove, N., Woodgett, J. R. and Lassam, N. J. 1996. MLK-3 activates the SAPK/JNK and p38/RK pathways via SEK1 and MKK3/6. EMBO J. 15:7026.
37. 2-terminal kinase 1 and MKK3/p38 pathways regulated by MEK kinases 2 and 3. J. Biol. Chem. 272:14489.
38. Ellinger-Ziegelbauer, H., Brown, K. and Siebenlist, U. 1997. Direct activation of the stress-activated protein kinase (SAPK) and extracellular signal-regulated protein kinase (ERK) pathways by an inducible mitogen-activated protein kinase/ERK kinase kinase 3 (MEKK) derivative. J. Biol. Chem. 272:2668.
39. 2-terminal kinase, activation correlates with surface IgM-mediated apoptosis in the WEHI-231 B cell line. J. Immunol. 161:1637.
40. Hacker, H., Mischak, H., Miethke, T., Liptay, S., Schmid, R., Sparwasser, T., Heeg, K., Lipford, G. B. and Wagner, H. 1998. CpG DNA specific activation of antigen presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J. 17:6230.
41. Bennett, B. L., Sasaki, D. T., Murray, B. W., O'Leary, E. C., Sakata, S. T., Xu, W., Leisten, J. C., Motiwala, A., Pierce, S., Satoh, Y., Bhagwat, S. S., Manning, A. M. and Anderson, D. W. 2001. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl Acad. Sci. USA 98:13681.
42. Richards, J. D., Dave, S. H., Chou, C.-H. G., Mamchak, A. A. and Defranco, A. L. 2001. Inhibition of the MEK/ERK signaling pathway blocks a subset of B cell response to antigen. J. Immunol. 166:3855.
43. 1 arrest in B lymphoma cells overexpressing dominant-negative mutant form of c-Jun N-terminal kinase 1. J. Immunol. 166:1641.
44. Chelvarajan, R. L., Raithatha, R., Venkataraman, C., Kaul, R., Han, S. S., Robertson, D. A. and S. Bondada. 1999. CpG oligodeoxynucleotides overcome the unresponsiveness of neonatal B cells to stimulation with the thymus-independent stimuli anti-IgM and TNP-Ficoll. Eur. J. Immunol. 29:2808.
45. Han, S. S., Chung, S. T., Robertson, D. A., Chelvarajan, R. L. and Bondada, S. 1999. CpG oligodeoxynucleotides rescue BKS-2 immature B cell lymphoma from anti-IgM-mediated growth inhibition by up-regulation of egr-1. Int. Immunol. 11:871.
46. Jego, G., Bataille, R. and Pellat-Deceunynck, C. 2001. Interleukin-6 is a growth factor for nonmalignant human plasmablasts. Blood 15:1817.
47. Yen Chong, S., Lin, Y. C., Czarneski, J., Zhang, M., Coffman, F., Kashanchi, F. and Raveche, E. 2001. Cell cycle effects of IL-10 on malignant B-1 cells. Genes Immun. 2:239.
48. Bajpai, U. D., Zhang, K., Teutsch, M., Sen, R. and Wortis, H. H. 2000. Bruton's tyrosine kinase links the B cell receptor to nuclear factor κB activation. J. Exp. Med. 191:1735.
49. Petro, J. B., Rahman, S. M. J., Ballard, D. W. and Khan, W. N. 2000. Bruton's tyrosine kinase is required for activation of IκB kinase and nuclear factor κB in response to B cell receptor engagement. J. Exp. Med. 191:1745.
50. Petro, J. B. and Khan, W. N. 2001. Phospholipase C-γ2 couples bruton's tyrosine kinase to the NF-κB signaling pathway in B lymphocytes. J. Biol. Chem. 276:1715.
51. Tan, J. E.-L., Wong, S.-C., Gan, S. K.-E., Xu, S. and Lam, K.-P. 2001. The adaptor protein BLNK is required for B cell antigen receptor-induced activation of nuclear factor-κB and cell cycle entry and survival of B lymphocytes. J. Biol. Chem. 276:20055.
52. Macfarlane, D. E., Manzel, L. and Krieg, A. M. 1997. Unmethylated CpG-containing oligodeoxynucleotides inhibit apoptosis in WEHI-231 B lymphocytes induced by several agents: evidence for blockade of apoptosis at a distal signaling step. Immunology 91:586.
53. Hacker, H., Vabulas, R. M., Takeuchi, O., Hoshino, K., Akira, S. and Wagner, H. 2000. Immune cell activation by bacterial CpG-DNA through myeloid differentiation marker 88 and tumor necrosis factor receptor-associated factor (TRAF)6. J. Exp. Med. 192:595.
54. Bauer, S., Kirschning, C. J., Häcker, H., Redecke, V., Hausmann, S., Akira, S., Wagner, H. and Lipford, G. B. 2001. Human TLR9 confers, responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl Acad. Sci. USA 98:9237.
55. Takeshita, F., Leifer, C. A., Gursel, I., Ishii, K. J., Takeshita, S., Gursel, M. and Klinman, D. M. 2001. Role of Toll-like receptor 9 in CpG DNA-induced activation of human cells. J. Immunol. 167:3555.
56. Hacker, H., Mischak, H., Hacker, G., Eser, S., Prenzel, N., Ullrich, A. and Wagner, H. 1999. Cell type-specific activation of mitogen-activated protein kinases by CpG-DNA controls interleukin-12 release from antigen-presenting cells. EMBO J. 18:6973.
57. Redford, T. W., Yi, A.-K., Ward, C. T. and Krieg, A. M. 1998. Cyclosporin A enhances IL-12 production by CpG motifs in bacterial DNA and synthetic oligodeoxynucleotides. J. Immunol. 161:3930.
58. Clipstone, N. A. and Crabtree, G. R. 1992. Identification of calcineurin as a key signaling enzyme in T-lymphocyte activation. Nature 357:695.
59. Fruman, D. A., Klee, C. B., Bierer, B. E. and Buralkoff, S. J. 1992. Calcineurin phosphatase activity in T lymphocytes is inhibited by FK 506 and cyclosporine A. Proc. Natl Acad. Sci. USA 89:3686.